Turk J Zool Research Article 33 (2009) 73-81 © TÜBİTAK doi:10.3906/zoo-0803-1

Some Turkish Species Studied Using Light and Scanning Electron Microscopy

Ahmet ALTINDAĞ1, Hendrik SEGERS2, Murat KAYA1,* 1Department of Biology, Faculty of Science, Ankara University, 06100 Beşevler, Ankara - TURKEY 2Royal Belgian Institute of Natural Sciences, Freshwater Biology, Vautierstraat 29, B-1000, Brussels, BELGIUM

Received: 05.03.2008

Abstract: A number of records of from Turkey are discussed. An account is given on trophi morphology in 4 species of Gosse, 1850. segersi De Smet, 1998 is recorded for the second time after its description, and Lecane shieli Segers and Sanoamuang, 1994 is recorded from Turkey for the first time. Both these and a population of Hexarthra polyodonta polyodonta (Hauer, 1957) from the species’ type locality, Lake Van, are illustrated using light and scanning electron microscopic techniques.

Key Words: Rotifera, trophi morphology, new records, Asplanchna, Cephalodella, Hexarthra, Turkey

Işık ve Taramalı Elektron Mikroskobu Kullanarak Bazı Türkiye Rotifer Tür Çalışmaları

Özet: Türkiye’den kaydedilen çok sayıda rotifer tartışıldı. Asplanchna Gosse, 1850’nin dört türünün trophi morfolojisi üzerine bir bilgi verildi. Cephalodella segersi De Smet, 1998 tanımlandığından sonra ikinci kez ve Lecane shieli Segers and Sanoamuang, 1994 ise Türkiye’den ilk kez kaydedildi. Hexarthra polyodonta polyodonta (Hauer, 1957)’nın bir populasyonu tip lokalitesinden ve diğer iki tür, ışık ve taramalı elektron mikroskobu (SEM) teknikleri kullanılarak şekillendirildi.

Anahtar Sözcükler: Rotifera, trophi morfolojisi, yeni kayıtlar, Asplanchna, Cephalodella, Hexarthra, Türkiye

Introduction According to José de Paggi (2002), the family The rotifer fauna of Turkey is relatively well known contains 15 species, 7 of which have been recorded from Turkey: Asplanchna brightwellii Gosse, (Ustaoğlu, 2004; Kaya et al., 2008), resulting in a total 1850; A. girodi de Guerne, 1888; A. priodonta Gosse, of 261 taxa recorded from the country. Nevertheless, it is 1850; A. sieboldii (Leydig, 1854); A. silvestrii Daday, clear that this figure is still far from complete: there are 1902; Asplanchnopus dahlgreni Myers, 1934; and A. only a few studies on the littoral and none on interstitial hyalinus Harring, 1913 (see Ustaoğlu, 2004; Erdoğan habitats of the region. As these are known to contain a and Güher, 2005). Numerous studies dealing with aspects highly diverse and specialised fauna, we expect that our of the of the genus Asplanchna are available knowledge of the α-diversity of aquatic ecosystems in the (e.g., Salt et al., 1978; Gilbert et al., 1979; Koste and region is, at best, incomplete. The new records presented Shiel, 1980; Pourriot et al., 1984; Koste and Tobias, herein illustrate this. 1988; Shiel and Koste, 1993; José de Paggi, 2002); One genus of pelagic rotifers that has been recorded however, the diversity in the trophi morphology of these quite frequently worldwide is Asplanchna Gosse, 1850. is still insufficiently documented.

* E-mail: [email protected]

73 Some Turkish Rotifer Species Studied Using Light and Scanning Electron Microscopy

Materials and Methods Our specimens have a vitellarium containing 47-53 nuclei, Samples were collected using a 55-μm-mesh plankton and the trophi lack lamellae behind the rami apices. They net and preserved in 4% formalin. We used Leica DMLS are also relatively small (female body length 428-621 μm, and Olympus BX51 microscopes for identification and trophi 135-178 μm, fulcrum 21-23 μm versus body drawing of the species. Trophi were isolated by dissolving length 800-1150 μm in José de Paggi (2002). the soft body parts in dilute NaOCl, and were prepared Notwithstanding these differences, we tentatively identify for scanning electron microscopy (SEM) following the the specimens as Asplanchna silvestrii, considering that procedure of De Smet (1998a). SEM was performed Salt et al. (1978) identified similar specimens lacking using a JEOL JSM-60 60 LV on material processed with a lamellae behind the rami apices as such. Polaron SC 502 sputter-coater. Sampling locality: the Turkish specimens are from Lake Akşehir (ecology: inland freshwater, Konya, Turkey), and were collected from the pelagic zone in May Results and Discussion 1993. Lake Akşehir is a tectonic lake, and has a maximum Here, we report the results of a taxonomic study of surface of 35,000 ha. The deepest part of the lake is 7 m some rare Turkish rotifer species (Asplanchna deep. Coordinates: 38°26’52.89”N, 31°25’26.66”E; brightwellii, A. girodi, A. priodonta, Asplanchna silvestrii, altitude: 966 m (Altınsaçlı et al., 2000). This species, Cephalodella segersi, Hexarthra polyodonta polyodonta, which is not uncommon in the Americas, appears to be and Lecane shieli). Two of these, Cephalodella segersi and rare in the Old World. Lecane shieli, are of particular biogeographic relevance Asplanchna brightwellii Gosse, 1850 (Figures 9-15): and are new to the Turkish fauna. Vitellarium horseshoe-shaped containing 23-31 nuclei. Morphology of some Turkish Asplanchna species Our specimens are relatively small: Female body length Identification of Asplanchna species relies on 260-430 μm, trophi 133-197 μm, fulcrum 15-19 μm anatomical features as well as on trophi morphology (see versus body length 500-1500 μm, trophi 130-270 μm, in José de Paggi, 2002). Our material presents an extension José de Paggi (2002). of the known variability in several species: Asplanchna brightwellii resembles A. sieboldii, and Asplanchna silvestrii Daday, 1902 (Figures 1-8) has a these 2 species have often been confused. However, their horseshoe-shaped vitellarium containing 38-42 nuclei and trophi are diagnostic: those of A. brightwellii have has trophi bearing large lamellae behind the rami apices symmetrical lamellae behind the rami apices, whereas (Sarma and Elias-Guttierez, 1997; José de Paggi, 2002). those in A. sieboldii are asymmetrical. 25 µm

100 µm 15 µm 123

Figures 1-3. Asplanchna silvestrii. 1: habitus (contracted specimens), 2: vitellarium, 3: trophus. 1, 2: ventral view, 3: dorsal view.

74 A. ALTINDAĞ, H SEGERS, M KAYA

20 µm 5 4 20 µm 6 20 µm

7 8

5 µm 10 µm

Figures 4-8. Trophi of Asplanchna silvestrii, SEM photographs. 4, 5, 7: dorsal view, 6, 8: ventral view.

50 µm

11

50 µm 50 µm 10 100 µm 9 12

Figures 9-12. Asplanchna brightwellii. 9: habitus (contracted specimens), 10. trophus, 11, 12: vitellarium. 9, 11, 12: ventral view, 10: dorsal view.

75 Some Turkish Rotifer Species Studied Using Light and Scanning Electron Microscopy

Sampling locality: The material originates from Sampling locality: The samples were collected from the Sarımsaklı Dam Lake (Kayseri, Turkey), collected on 30 pelagic part of Ağcaşar Dam Lake (Kayseri, Turkey), on 25 August 2006. The samples were collected from the December 2005. Coordinates: 38°10’41.71”N, pelagic part of the lake. Coordinates: 38°53’16.50”N, 35°23’39.39”E; altitude: 292 m, ecology: alkali inland water. 35°44’26.30”E; altitude: 1330 m, ecology: inland Asplanchna girodi de Guerne, 1888 (Figures 19-21): freshwater. Our specimens are relatively small compared to the Asplanchna priodonta Gosse, 1850 (Figures 16-18): recorded range for the species [Female body length 453- The size of the specimens falls within the range given for 522 μm, trophi 78-89 μm, fulcrum 15-17 μm, versus the species by José de Paggi (2002): Female body length body length 500-700 μm, males 250-397 μm, trophi 93 479-553 μm, trophi 63-74 μm, fulcrum 14-16 μm. μm in José de Paggi (2002)].

r im

t s m b a

sa 10 μm 20 μm 13 10 μm 14 f 15

Figures 13-15. SEM trophi of Asplanchna brightwellii (a: apophysis, b: bulla, f: fulcrum, im: inner margin of the ramus, m: manubrium, r: ramus, s: scapus, sa: subapophysis, t: tooth of the ramus).

100 µm 50 µm

16 17 Figures 16, 17. Asplanchna priodonta. 16: habitus; 17: trophus. 16, 17: dorsal view.

76 A. ALTINDAĞ, H SEGERS, M KAYA

Sampling locality: The samples are from Sarıkamış (Kars, Turkey), 16 July 1986 (coll. H. J. Dumont). Coordinates: 40°19’52.78”N, 42°34’43.14”E; altitude: 2750 m, ecology: inland freshwater. As far as can be judged from published records, Asplanchna sieboldii appears to be slightly more common in Turkey than A. brightwellii: A. sieboldii has been recorded from 11 different localities (Geldiay, 1949; Margaritora et al., 1977; Segers et al., 1992; Altındağ and Yiğit, 1999; Bekleyen, 2001; Bozkurt et al., 2002; Erdoğan and Güher, 2005; Bozkurt, 2006; Kaya and Altındağ, 2007), whereas A. brightwellii has been recorded from 7 localities, including the present study (Daday, 1903; Mann, 1940; Geldiay, 1949; Margaritora and Cottarelli, 1970; Dumont and De Ridder, 1987). This assessment is preliminary, however, as they have been 10 µm confused in the past. We hope that the present illustration of their trophi, and of those of the other species, will prevent further confusion. Other new or rare Turkish rotifers

18 Cephalodella segersi De Smet, 1998 (Figures 22-25): This species’ habitus, and toe and trophi shape indicate a close relationship with Cephalodella catellina (Müller, Figure 18. SEM trophus of A. priodonta. Ventral view. 1786) (De Smet, 1998b). They are easily distinguished, however, by their characteristic trophi: in C. segersi the right manubrium has an incompletely closed terminal loop

50 µm

100 µm

19 20

Figures 19, 20. Asplanchna girodi. 19: habitus, 20: trophus. 19: ventral view, 20: dorsal view.

77 Some Turkish Rotifer Species Studied Using Light and Scanning Electron Microscopy

with a forked ventral arm; its left manubrium ends in an open loop with a simple ventral arm (Figures 24, 25). In C. catellina both manubria end in an incompletely closed loop with a simple ventral arm. C. segersi is furthermore la characterised by having a more prominent alula on its left ramus, and the less developed basal chamber of the right ramus (see De Smet, 1998b for more details). The Turkish specimens are slightly larger than those recorded from Belgium by De Smet (1998b). Our measurements indicate a total length of 77-109 μm, toe length 15-17 μm, total trophi length of 30 μm (fulcrum 10 µm 19 μm, left uncus 20 μm, right uncus 17 μm), whereas De Smet (1998b) records a total length of 68-98 μm, toe length 15-18 μm, and trophi 22-23 μm. 21 Even though confusion with any other of its 154 congeners (Segers, 2007) is hardly possible considering the highly characteristic trophi of C. segersi (Nogrady et Figure 21. SEM trophus of A. girodi. Ventral view (la: lamellae). al., 1995; see De Smet, 1998b), it is likely that the

22 23 50 µm

lm

rm

dm

24 5 µm 25

Figures 22-25. Cephalodella segersi. 22, 23: habitus, 24, 25: trophi (22, 23: lateral views, 24, 25: dorso-lateral views, dm: distal manubria part, lm: left manubrium, rm: right manubrium).

78 A. ALTINDAĞ, H SEGERS, M KAYA

species has been overlooked in the past. Cephalodella trophi 29 μm, width of trophi 47 μm, fulcrum 7 μm, segersi was described from man-made Lake Blankaart, ramus 21 μm. This species is known in Turkey from 2 near the outlet of “Steenbeek” rivulet, Woumen, West localities only (Dumont and De Ridder, 1987). We hope Vlaanderen, Belgium. that our SEM examination of the trophi of the population Sampling locality: the Turkish specimens are from from the type locality of the taxon may help to clarify the Lake Yeniçağ (Bolu, Turkey) and were collected on 13 status of the 2 subspecies of H. polyodonta, viz. H. July 2005. They represent the second record of the polyodonta soaplakeiensis Koste, 1977 and H. polyodonta species. Coordinates: 40°42’7.05”N, 31°31’43.08”E; jasperina Dumont, Coussement and Anderson, 1978, and altitude: 900 m, inland freshwater. contribute to a better understanding of the taxon’s distribution. Hexarthra polyodonta polyodonta (Hauer, 1957) (Figures 26-32): the number of the uncus teeth is 11-13. Sampling locality: the specimens examined are from Total measurements: body length 364 μm, length of the species’ type locality, Lake Van (Van, Turkey; Hauer,

26 27

50 μm 50 μm

10 µm 28 29 10 µm

r u

5 µm 5 µm m 5 µm 30 31 32

Figures 26-32. Hexarthra polyodonta. 26: habitus, 27: vental arm, 28: apical view of trophi, 29: posterior view of trophi, 30, 32: posterior views of manubrium and uncus, 31: ventral view of rami (f: fulcrum, m: manubrium, r: ramus, u: uncus teeth).

79 Some Turkish Rotifer Species Studied Using Light and Scanning Electron Microscopy

1957), and were collected on 12 July 2003. Coordinates: and Yiğit, 2005), the species is unmistakable by its 38°28’4.51”N, 43°15’19.17”E; altitude: 1026 m, relatively soft yet elongate and nearly parallel-sided lorica, ecology: saline lake. and long toes with curved claws. It is similar to L. Lecane shieli Segers and Sanoamuang, 1994 (Figure isanensis Sanoamuang and Savatenalinton, 2001, but the 33). To date, this species has only been recorded from latter species lacks antero-lateral head aperture spines. several localities in Thailand (e.g., Sanoamuang and The present specimens, although appearing different Savatenalinton, 2001), and has recently been recorded morphologically because they are relatively weakly from Australia (Kobayashi et al., 2007). Although Lecane contracted, clearly belong to this species and represent shieli can be confused with L. elegans (e.g., by Altındağ the first record of the taxon outside Thailand and Australia. The size of the Turkish specimens (dorsal plate length 98-103, width 61, ventral plate length 110-118, toe length 43.5-47, claw length 6.7-8.6 μm) concurs with the range given for the species by Segers and 33 Sanoamuang (1994). Sampling locality: The Turkish specimens were collected from Beyşehir Lake on 21 November 2000 (Konya, Turkey). Coordinates: 37°41’48.51”N, 31°37’34.10”E; altitude: 1125 m, ecology: alkali lake.

Conclusion

50 µm As a result of this study, we add 2 species to the list of Turkish rotifers, and the presence of Asplanchna silvestrii, a species that is particularly rare in the Old World and rather common in the Americas, is confirmed. The total diversity of rotifers in Turkey herewith stands at 263 species. The SEM study of trophi in Asplanchna will hopefully clear up the uncertainty regarding species identifications in the genus.

Acknowledgements The authors would like to thank Dr S. José de Paggi and Dr R.J. Shiel for comments and suggestions. The authors would like to thank Prof. Dr. Yusuf Kalender and technician Yusuf Erdemir (Department of Biology, Gazi University in Turkey) for access to the scanning electron Figure 33. Lecane shieli habitus, ventral view. microscope.

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